Identifying and targeting cancer stem cells in leiomyosarcoma: prognostic impact and role to overcome secondary resistance to PI3K/mTOR inhibition

J Hematol Oncol. 2019 Jan 25;12(1):11. doi: 10.1186/s13045-018-0694-1.

Abstract

Background: Leiomyosarcoma (LMS) is one of the most frequent soft tissue sarcoma subtypes and is characterized by a consistent deregulation of the PI3K/mTOR pathway. Cancer stem cells (CSCs) have been poorly studied in soft tissue sarcomas. In this study, we aimed to evaluate the association between CSCs, the outcome of LMS patients, and the resistance to PI3K/mTOR pathway inhibition.

Methods: We investigated the relationships between aldehyde dehydrogenase 1 (ALDH1) expression, a cancer stem cell marker, and the outcome of LMS patients in two independent cohorts. We assessed the impact of CSCs in resistance to PI3K/mTOR pathway inhibition using LMS cell lines, a xenograft mouse model, and human tumor samples.

Results: We found that enhanced ALDH1 activity is a hallmark of LMS stem cells and is an independent prognostic factor. We also identified that secondary resistance to PI3K/mTOR pathway inhibition was associated with the expansion of LMS CSCs. Interestingly, we found that EZH2 inhibition, a catalytic component of polycomb repressive complex which plays a critical role in stem cell maintenance, restored sensitivity to PI3K/mTOR pathway inhibition. Importantly, we confirmed the clinical relevance of our findings by analyzing tumor samples from patients who showed secondary resistance after treatment with a PI3Kα inhibitor.

Conclusions: Altogether, our findings suggest that CSCs have a strong impact on the outcome of patients with LMS and that combining PI3K/mTOR and EZH2 inhibitors may represent a promising strategy in this setting.

Keywords: ALDH1; BEZ235; Cancer stem cell; EZH2; Leiomyosarcoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aldehyde Dehydrogenase 1 Family / metabolism
  • Animals
  • Cell Line, Tumor
  • Cohort Studies
  • Drug Resistance, Neoplasm*
  • Enhancer of Zeste Homolog 2 Protein / antagonists & inhibitors
  • Female
  • Humans
  • Imidazoles / pharmacology
  • Imidazoles / therapeutic use
  • Leiomyosarcoma / drug therapy
  • Leiomyosarcoma / metabolism*
  • Leiomyosarcoma / pathology*
  • Male
  • Mice
  • Mice, Inbred NOD
  • Mice, Knockout
  • Mice, SCID
  • Middle Aged
  • Neoplastic Stem Cells / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Phosphoinositide-3 Kinase Inhibitors / pharmacology
  • Phosphoinositide-3 Kinase Inhibitors / therapeutic use
  • Prognosis
  • Protein Kinase Inhibitors / therapeutic use
  • Quinolines / pharmacology
  • Quinolines / therapeutic use
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Imidazoles
  • Phosphoinositide-3 Kinase Inhibitors
  • Protein Kinase Inhibitors
  • Quinolines
  • Aldehyde Dehydrogenase 1 Family
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • MTOR protein, human
  • TOR Serine-Threonine Kinases
  • dactolisib